Cumulative effects of ocean acidification, eutrophication, and competition on the growth of two bloom-forming, estuarine macroalgae

While there is a growing interest in understanding how marine life will respond to future ocean acidification, many coastal ecosystems currently experience intense acidification in response to upwelling, riverine discharge, and eutrophication. Such acidification can be inhibitory to calcifying animals, but less is known regarding how non-calcifying macro algae may respond to elevated CO2. Additionally, while the ability of some marine autotrophs to benefit from elevated CO2 over others may result in shifts in community structure, such shifts can also be affected by competition between primary producers. In order to examine what role ocean acidification, eutrophication, and competition plays in the growth of marine macroalgae, a series of experiments were performed during summer through fall 2014 and 2015 with North Atlantic populations of Gracilaria tikvahiae and Ulva rigida that were grown in situ within a mesotrophic estuary (Shinnecock Bay, NY, USA) or exposed to normal and elevated, but environmentally realistic, levels of pCO2 and/or nutrients (nitrogen and phosphorus), as well as being subjected to competition with each other as well as with diatom and dinoflagellate assemblages (2015). Across the 2014 and 2015 experiments, the growth rates of Gracilaria were significantly increased by 70% (2014) and 34% (2015) when exposed to elevated levels of pCO2 (p<0.05). Under the same conditions, the growth rates of Ulva were increased by 30% (2014) and 41% (2015). For nearly all 2014 experiments, Gracilaria was unaffected by nutrient enrichment. In contrast, the growth response of Ulva was more complex as this alga experienced significantly (p<0.05) increased growth rates in response to both elevated pCO2 and nutrients and, in two cases, pCO2 and nutrients interacted to provide synergistically enhanced growth. For the 2015 experiments, growth rates of Gracilaria with or without elevated pCO2 were unaffected by the presence of competing plankton or Ulva. In contrast, growth of Ulva was significantly reduced when grown with Gracilaria (p<0.05) and in several experiments, growth rates of Ulva were found to be significantly reduced when competing with plankton (p<0.05). Dinoflagellates grew significantly faster when exposed to elevated pCO2 (p<0.05) but experienced significantly reduced growth rates grown with Gracilaria (p<0.05). Across all experiments, Gracilaria and Ulva experienced significant declines in tissue δ13C signatures, suggesting that increased growth rates were associated with a shift from use of HCO3- to CO2 use. This shift in carbon use coupled with significantly increased growth in response to elevated pCO2 suggests that photosynthesis of these algae was limited by their inorganic carbon supply. For the 2015 experiments, elevated C:N ratios among macroalgae suggested that competition for N also shaped interactions among autotrophs, particularly for Ulva. Collectively, these study demonstrates that while several types of estuarine autotrophs can benefit from elevated pCO2 levels, their relative benefit can change when direct competition with other primary producers is considered with Gracilaria outcompeting Ulva and dinoflagellates outcompeting diatoms under high pCO2.